Learning from structure-based drug design and new antivirals targeting the ribonucleoprotein complex for the treatment of influenza

Bibliography

• Dunning J, Baillie JK, Cao B, et al. Antiviral combinations for severe influenza. Lancet Infect Dis 2014;14(12):1259-70
   PubMed Web of Science ®Google Scholar
• Du J, Cross TA, Zhou HX. Recent progress in structure-based anti-influenza drug design. Drug Discov Today 2012;17(19-20):1111-20
   PubMed Web of Science ®Google Scholar
• Wang J, Wu Y, Ma C, et al. Structure and inhibition of the drug-resistant S31N mutant of the M2 ion channel of influenza A virus. Proc Natl Acad Sci USA 2013;110(4):1315-20
   PubMed Web of Science ®Google Scholar
• Das K. Antivirals targeting influenza a virus. J Med Chem 2012;55:6263-77
   PubMed Web of Science ®Google Scholar
• Das K, Aramini JM, Ma LC, et al. Structures of influenza A proteins and insights into antiviral drug targets. Nat Struct Mol Biol 2010;17(5):530-8
   PubMed Web of Science ®Google Scholar
• Loregian A, Mercorelli B, Nannetti G, et al. Antiviral strategies against influenza virus: towards new therapeutic approaches. Cell Mol Life Sci 2014;71(19):3659-83
   PubMed Web of Science ®Google Scholar
• Muller KH, Kakkola L, Nagaraj AS, et al. Emerging cellular targets for influenza antiviral agents. Trends Pharmacol Sci 2012;33(2):89-99
   PubMed Web of Science ®Google Scholar
• Smee DF, Bailey KW, Wong MH, et al. Treatment of influenza A (H1N1) virus infections in mice and ferrets with cyanovirin-N. Antiviral Res 2008;80(3):266-71
   PubMed Web of Science ®Google Scholar
• Brancato V, Peduto A, Wharton S, et al. Design of inhibitors of influenza virus membrane fusion: synthesis, structure-activity relationship and in vitro antiviral activity of a novel indole series. Antiviral Res 2013;99(2):125-35
   PubMed Web of Science ®Google Scholar
• Leneva IA, Russell RJ, Boriskin YS, et al. Characteristics of arbidol-resistant mutants of influenza virus: implications for the mechanism of anti-influenza action of arbidol. Antiviral Res 2009;81(2):132-40
   PubMed Web of Science ®Google Scholar
• Russell RJ, Kerry PS, Stevens DJ, et al. Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc Natl Acad Sci USA 2008;105(46):17736-41
   PubMed Web of Science ®Google Scholar
• Tang G, Lin X, Qiu Z, et al. Design and synthesis of benzenesulfonamide derivatives as potent anti-influenza hemagglutinin inhibitors. ACS Med Chem Lett 2011;2(8):603-7
   PubMed Web of Science ®Google Scholar
• Fleishman SJ, Whitehead TA, Ekiert DC, et al. Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 2011;332(6031):816-21
   PubMed Web of Science ®Google Scholar
• Basu A, Antanasijevic A, Wang M, et al. New small molecule entry inhibitors targeting hemagglutinin-mediated influenza a virus fusion. J Virol 2014;88(3):1447-60
   PubMed Web of Science ®Google Scholar
• Kim CU, Lew W, Williams MA, et al. Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site: design, synthesis, and structural analysis of carbocyclic sialic acid analogues with potent anti-influenza activity. J Am Chem Soc 1997;119(4):681-90
   PubMed Web of Science ®Google Scholar
• Russell RJ, Haire LF, Stevens DJ, et al. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 2006;443(7107):45-9
   PubMed Web of Science ®Google Scholar
• Spanakis N, Pitiriga V, Gennimata V, Taskris A. A review of neuraminidase inhibitor susceptibility in influenza strains. Expert Rev Anti Infect Ther 2014;12:1325-36
   PubMed Web of Science ®Google Scholar
• Vavricka CJ, Li Q, Wu Y, et al. Structural and functional analysis of laninamivir and its octanoate prodrug reveals group specific mechanisms for influenza NA inhibition. PLoS Pathog 2011;7(10):e1002249
   PubMed Web of Science ®Google Scholar
• Ivachtchenko AV, Ivanenkov YA, Mitkin OD, et al. Novel oral anti-influenza drug candidate AV5080. J Antimicrob Chemother 2014;69(7):1892-902
   PubMed Web of Science ®Google Scholar
• Vavricka CJ, Liu Y, Kiyota H, et al. Influenza neuraminidase operates via a nucleophilic mechanism and can be targeted by covalent inhibitors. Nat Commun 2013;4:1491
   PubMed Web of Science ®Google Scholar
• Kim JH, Resende R, Wennekes T, et al. Mechanism-based covalent neuraminidase inhibitors with broad-spectrum influenza antiviral activity. Science 2013;340(6128):71-5
   PubMed Web of Science ®Google Scholar
• Rudrawar S, Dyason JC, Rameix-Welti MA, et al. Novel sialic acid derivatives lock open the 150-loop of an influenza A virus group-1 sialidase. Nat Commun 2010;1:113
   PubMed Web of Science ®Google Scholar
• Mohan S, Kerry PS, Bance N, et al. Serendipitous discovery of a potent influenza virus a neuraminidase inhibitor. Angew Chem Int Ed Engl 2014;53(4):1076-80
   PubMed Web of Science ®Google Scholar
• Kerry PS, Mohan S, Russell RJ, et al. Structural basis for a class of nanomolar influenza A neuraminidase inhibitors. Sci Rep 2013;3:2871
   PubMed Web of Science ®Google Scholar
• Lee CM, Weight AK, Haldar J, et al. Polymer-attached zanamivir inhibits synergistically both early and late stages of influenza virus infection. Proc Natl Acad Sci USA 2012;109(50):20385-90
   PubMed Web of Science ®Google Scholar
• Schnell JR, Chou JJ. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 2008;451(7178):591-5
   PubMed Web of Science ®Google Scholar
• Cady SD, Schmidt-Rohr K, Wang J, et al. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 2010;463(7281):689-92
   PubMed Web of Science ®Google Scholar
• Gu RX, Liu LA, Wei DQ. Structural and energetic analysis of drug inhibition of the influenza A M2 proton channel. Trends Pharmacol Sci 2013;34(10):571-80
   PubMed Web of Science ®Google Scholar
• Duque MD, Ma C, Torres E, et al. Exploring the size limit of templates for inhibitors of the M2 ion channel of influenza A virus. J Med Chem 2011;54(8):2646-57
   PubMed Web of Science ®Google Scholar
• Chenavas S, Estrozi LF, Delmas B, et al. Monomeric nucleoprotein of Influenza A virus. Plos Pathogens 2013;9(3):e1003275
   PubMed Web of Science ®Google Scholar
• Cianci C, Gerritz SW, Deminie C, et al. Influenza nucleoprotein: promising target for antiviral chemotherapy. Antivir Chem Chemother 2012;23(3):77-91
   Google Scholar
• Davis AM, Chabolla BJ, Newcomb LL. Emerging antiviral resistant strains of influenza A and the potential therapeutic targets within the viral ribonucleoprotein (vRNP) complex. Virol J 2014;11:167
   PubMedGoogle Scholar
• Arranz R, Coloma R, Chichon FJ, et al. The structure of native influenza virion ribonucleoproteins. Science 2012;338(6114):1634-7
   PubMed Web of Science ®Google Scholar
• Moeller A, Kirchdoerfer RN, Potter CS, et al. Organization of the influenza virus replication machinery. Science 2012;338(6114):1631-4
   PubMed Web of Science ®Google Scholar
• Coloma R, Valpuesta JM, Arranz R, et al. The structure of a biologically active influenza virus ribonucleoprotein complex. PLoS Pathog 2009;5(6):e1000491
   PubMed Web of Science ®Google Scholar
• Ng AK, Chan WH, Choi ST, et al. Influenza Polymerase Activity Correlates with the Strength of Interaction between Nucleoprotein and PB2 through the Host-Specific Residue K/E627. PLoS ONE 2012;7(5):e36415
   PubMedGoogle Scholar
• Marklund JK, Ye Q, Dong J, et al. Sequence in the influenza A virus nucleoprotein required for viral polymerase binding and RNA synthesis. J Virol 2012;86(13):7292-7
   PubMed Web of Science ®Google Scholar
• Gui X, Li R, Zhang X, et al. An important amino acid in nucleoprotein contributes to influenza A virus replication by interacting with polymerase PB2. Virology 2014;464-465:11-20
   PubMed Web of Science ®Google Scholar
• Gavazzi C, Yver M, Isel C, et al. A functional sequence-specific interaction between influenza A virus genomic RNA segments. Proc Natl Acad Sci USA 2013;110(41):16604-9
   PubMed Web of Science ®Google Scholar
• Turrell L, Lyall JW, Tiley LS, et al. The role and assembly mechanism of nucleoprotein in influenza A virus ribonucleoprotein complexes. Nat Commun 2013;4:1591
   PubMed Web of Science ®Google Scholar
• Portela A, Digard P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol 2002;83(Pt 4):723-34
   PubMed Web of Science ®Google Scholar
• Newcomb LL, Kuo RL, Ye Q, et al. Interaction of the influenza a virus nucleocapsid protein with the viral RNA polymerase potentiates unprimed viral RNA replication. J Virol 2009;83(1):29-36
   PubMed Web of Science ®Google Scholar
• Ruigrok RW, Baudin F. Structure of influenza virus ribonucleoprotein particles. II. Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles. J Gen Virol 1995;76(Pt 4):1009-14
   PubMedGoogle Scholar
• Ng AK, Zhang H, Tan K, et al. Structure of the influenza virus A H5N1 nucleoprotein: implications for RNA binding, oligomerization, and vaccine design. FASEB J 2008;22(10):3638-47
   PubMed Web of Science ®Google Scholar
• Ye Q, Krug RM, Tao YJ. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 2006;444(7122):1078-82
   PubMed Web of Science ®Google Scholar
• Ye Q, Guu TS, Mata DA, et al. Biochemical and structural evidence in support of a coherent model for the formation of the double-helical influenza A virus ribonucleoprotein. MBio 2012;4(1):e00467-12
   Google Scholar
• Ng AK, Lam MK, Zhang H, et al. Structural basis for RNA binding and homo-oligomer formation by influenza B virus nucleoprotein. J Virol 2012;86(12):6758-67
   PubMed Web of Science ®Google Scholar
• Ruigrok RW, Crepin T, Kolakofsky D. Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr Opin Microbiol 2011;14(4):504-10
   PubMed Web of Science ®Google Scholar
• Reguera J, Cusack S, Kolakofsky D. Segmented negative strand RNA virus nucleoprotein structure. Curr Opin Virol 2014;5:7-15
   PubMed Web of Science ®Google Scholar
• Reguera J, Malet H, Weber F, et al. Structural basis for encapsidation of genomic RNA by La Crosse Orthobunyavirus nucleoprotein. Proc Natl Acad Sci USA 2013;110(18):7246-51
   PubMed Web of Science ®Google Scholar
• Tarus B, Bakowiez O, Chenavas S, et al. Oligomerization paths of the nucleoprotein of influenza A virus. Biochimie 2012;94:776-85
   Web of Science ®Google Scholar
• Tarus B, Chevalier C, Richard CA, et al. Molecular dynamics studies of the nucleoprotein of influenza a virus: role of the protein flexibility in RNA binding. PLoS ONE 2012;7(1):e30038
   PubMedGoogle Scholar
• Boulo SA, Lotteau H, Mueller V, et al. Human importin alpha and RNA do not compete for binding to Influenza A nucleoprotein. Virology 2011;409(1):84-90
   PubMed Web of Science ®Google Scholar
• Amorim MJ, Kao RY, Digard P. Nucleozin targets cytoplasmic trafficking of viral ribonucleoprotein-Rab11 complexes in influenza A virus infection. J Virol 2013;87(8):4694-703
   PubMed Web of Science ®Google Scholar
• Kao RY, Yang D, Lau LS, et al. Identification of influenza A nucleoprotein as an antiviral target. Nat Biotechnol 2010;28(6):600-5
   PubMed Web of Science ®Google Scholar
• Cheng H, Wan J, Lin MI, et al. Design, synthesis, and in vitro biological evaluation of 1H-1,2,3-triazole-4-carboxamide derivatives as new anti-influenza A agents targeting virus nucleoprotein. J Med Chem 2012;55(5):2144-53
   PubMed Web of Science ®Google Scholar
• Gerritz SW, Cianci C, Kim S, et al. Inhibition of influenza virus replication via small molecules that induce the formation of higher-order nucleoprotein oligomers. Proc Natl Acad Sci USA 2011;108(37):15366-71
   PubMed Web of Science ®Google Scholar
• Shen YF, Chen YH, Chu SY, et al. E339 R416 salt bridge of nucleoprotein as a feasible target for influenza virus inhibitors. Proc Natl Acad Sci USA 2011;108(40):16515-20
   PubMed Web of Science ®Google Scholar
• Lejal N, Tarus B, Bouguyon E, et al. Structure-Based Discovery of the Novel Antiviral Properties of Naproxen against the Nucleoprotein of Influenza A Virus. Antimicrob Agents Chemother 2013;57(5):2231-42
   PubMed Web of Science ®Google Scholar
• Tarus B, Bertrand H, Zedda G, et al. Structure-based design of novel naproxen derivatives targeting monomeric nucleoprotein of Influenza A virus. J Biomol Struct Dyn 2014; [ Epub ahead of print
   Google Scholar
• Dias A, Bouvier D, Crepin T, et al. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 2009;458(7240):914-18
   PubMed Web of Science ®Google Scholar
• Yuan P, Bartlam M, Lou Z, et al. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 2009;458(7240):909-13
   PubMed Web of Science ®Google Scholar
• He X, Zhou J, Bartlam M, et al. Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 2008;454(7208):1123-6
   PubMed Web of Science ®Google Scholar
• Obayashi E, Yoshida H, Kawai F, et al. The structural basis for an essential subunit interaction in influenza virus RNA polymerase. Nature 2008;454(7208):1127-31
   PubMed Web of Science ®Google Scholar
• Sugiyama K, Obayashi E, Kawaguchi A, et al. Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. EMBO J 2009;28(12):1803-11
   PubMed Web of Science ®Google Scholar
• Guilligay D, Tarendeau F, Resa-Infante P, et al. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 2008;15(5):500-6
   PubMed Web of Science ®Google Scholar
• Tarendeau F, Crepin T, Guilligay D, et al. Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog 2008;4(8):e1000136
   PubMed Web of Science ®Google Scholar
• Pflug A, Guiigay D, Reich S, et al. Structure of influenza A polymerase bound to the viral RNA promoter. Nature 2014;516(7531):355-60.
   Google Scholar
• Reich S, Guilligay D, Malet H, et al. Structural insight into cap-snatching and RNA synthesis by influenza polymerase. Nature 2014;516(7531):361-6.
   Google Scholar
• Pautus S, Sehr P, Lewis J, et al. New 7-methylguanine derivatives targeting the influenza polymerase PB2 cap-binding domain. J Med Chem 2013;56(21):8915-30
   PubMed Web of Science ®Google Scholar
• Clark MP, Ledeboer MW, Davies I, et al. Discovery of a novel, first-in-class, orally bioavailable azaindole inhibitor (VX-787) of influenza PB2. J Med Chem 2014;57(15):6668-78
   PubMed Web of Science ®Google Scholar
• Wathen MW, Barro M, Bright RA. Antiviral in seasonal and pandemic influenza-future perspectives. Influenza Other Respir Viruses 2012;7(Suppl 1):76-80
   Google Scholar
• Bauman JD, Patel D, Baker SF, et al. Crystallographic fragment screening and structure-based optimization yields a new class of influenza endonuclease inhibitors. ACS Chem Biol 2013;8:2501-8
   PubMed Web of Science ®Google Scholar
• Kowalinski E, Zubieta C, Wolkerstorfer A, et al. Structural analysis of specific metal chelating inhibitor binding to the endonuclease domain of influenza pH1N1 (2009) polymerase. PLoS Pathog 2012;8(8):e1002831
   PubMed Web of Science ®Google Scholar
• DuBois RM, Slavish PJ, Baughman BM, et al. Structural and biochemical basis for development of influenza virus inhibitors targeting the PA endonuclease. PLoS Pathog 2012;8(8):e1002830
   PubMed Web of Science ®Google Scholar
• Parhi AK, Xiang A, Bauman JD, et al. Phenyl substituted 3-hydroxypyridin-2(1H)-ones: inhibitors of influenza A endonuclease. Bioorg Med Chem 2013;21(21):6435-46
   PubMed Web of Science ®Google Scholar
• Sagong HY, Bauman JD, Patel D, et al. Phenyl Substituted 4-Hydroxypyridazin-3(2H)-ones and 5-Hydroxypyrimidin-4(3H)-ones: inhibitors of Influenza A Endonuclease. J Med Chem 2014;57(19):8086-98
   PubMed Web of Science ®Google Scholar
• Sagong HY, Parhi A, Bauman JD, et al. 3-Hydroxyquinolin-2(1H)-ones As Inhibitors of Influenza A Endonuclease. ACS Med Chem Lett 2013;4(6):547-50
   PubMed Web of Science ®Google Scholar
• Tefsen B, Lu G, Zhu Y, et al. The N-terminal domain of PA from bat-derived influenza-like virus H17N10 has endonuclease activity. J Virol 2014;88(4):1935-41
   PubMed Web of Science ®Google Scholar
• Tomassini J, Selnick H, Davies ME, et al. Inhibition of cap (m7GpppXm)-dependent endonuclease of influenza virus by 4-substituted 2,4-dioxobutanoic acid compounds. Antimicrob Agents Chemother 1994;38(12):2827-37
   PubMed Web of Science ®Google Scholar
• Muratore G, Mercorelli B, Goracci L, et al. Human cytomegalovirus inhibitor AL18 also possesses activity against influenza A and B viruses. Antimicrob Agents Chemother 2012;56(11):6009-13
   PubMed Web of Science ®Google Scholar
• Muratore G, Goracci L, Mercorelli B, et al. Small molecule inhibitors of influenza A and B viruses that act by disrupting subunit interactions of the viral polymerase. Proc Natl Acad Sci USA 2012;109(16):6247-52
   PubMed Web of Science ®Google Scholar
• Pagano M, Castagnolo D, Bernardini M, et al. The fight against the influenza A virus H1N1: synthesis, molecular modeling, and biological evaluation of benzofurazan derivatives as viral RNA polymerase inhibitors. ChemMedChem 2014;9(1):129-50
   PubMed Web of Science ®Google Scholar
• Tintori C, Laurenzana I, Fallacara AL, et al. High-throughput docking for the identification of new influenza A virus polymerase inhibitors targeting the PA-PB1 protein-protein interaction. Bioorg Med Chem Lett 2014;24(1):280-2
   PubMed Web of Science ®Google Scholar
• Brownlee GG, Sharps JL. The RNA polymerase of influenza a virus is stabilized by interaction with its viral RNA promoter. J Virol 2002;76(14):7103-13
   PubMed Web of Science ®Google Scholar
• Fodor E, Crow M, Mingay LJ, et al. A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J Virol 2002;76(18):8989-9001
   PubMed Web of Science ®Google Scholar
• Perales B, Ortin J. The influenza A virus PB2 polymerase subunit is required for the replication of viral RNA. J Virol 1997;71(2):1381-5
   PubMed Web of Science ®Google Scholar
• Perez DR, Donis RO. Functional analysis of PA binding by influenza a virus PB1: effects on polymerase activity and viral infectivity. J Virol 2001;75(17):8127-36
   PubMed Web of Science ®Google Scholar
• Ghanem A, Mayer D, Chase G, et al. Peptide-mediated interference with influenza A virus polymerase. J Virol 2007;81(14):7801-4
   PubMed Web of Science ®Google Scholar
• Wunderlich K, Mayer D, Ranadheera C, et al. Identification of a PA-binding peptide with inhibitory activity against influenza A and B virus replication. PLoS ONE 2009;4(10):e7517
   PubMedGoogle Scholar
• Li C, Ba Q, Wu A, et al. A peptide derived from the C-terminus of PB1 inhibits influenza virus replication by interfering with viral polymerase assembly. FEBS J 2013;280(4):1139-49
   PubMed Web of Science ®Google Scholar
• Engel DA. The influenza virus NS1 protein as a therapeutic target. Antiviral Res 2013;99(3):409-16
   PubMed Web of Science ®Google Scholar
• Yin C, Khan JA, Swapna GV, et al. Conserved surface features form the double-stranded RNA binding site of non-structural protein 1 (NS1) from influenza A and B viruses. J Biol Chem 2007;282(28):20584-92
   PubMed Web of Science ®Google Scholar
• Cho EJ, Xia S, Ma LC, et al. Identification of influenza virus inhibitors targeting NS1A utilizing fluorescence polarization-based high-throughput assay. J Biomol Screen 2012;17(4):448-59
   PubMed Web of Science ®Google Scholar
• You L, Cho EJ, Leavitt J, et al. Synthesis and evaluation of quinoxaline derivatives as potential influenza NS1A protein inhibitors. Bioorg Med Chem Lett 2011;21(10):3007-11
   PubMed Web of Science ®Google Scholar
• Qin S, Liu Y, Tempel W, et al. Structural basis for histone mimicry and hijacking of host proteins by influenza virus protein NS1. Nat Commun 2014;5:3952
   PubMedGoogle Scholar
• Cencic R, Hall DR, Robert F, et al. Reversing chemoresistance by small molecule inhibition of the translation initiation complex eIF4F. Proc Natl Acad Sci USA 2011;108(3):1046-51
   PubMed Web of Science ®Google Scholar
• Chenavas S, Crepin T, Delmas B, et al. Influenza virus nucleoprotein: structure, RNA binding, oligomerization and antiviral drug target. Future Microbiol 2013;8:1537-45
   PubMed Web of Science ®Google Scholar